The “fruit and whole‐grain” pattern is associated with a low prevalence of hypertriglyceridemia among middle and older‐aged Korean adults: Using Korea National Health and Nutrition Examination Survey 2013–2018 data

Abstract Hypertriglyceridemia is a well‐known risk factor of various chronic diseases including diabetes mellitus, metabolic syndrome, obesity, and cardiovascular diseases. This study aimed to determine dietary patterns and explore the relationship between dietary patterns and hypertriglyceridemia in the Korean adult population. We utilized a cross‐sectional and nationally representative survey, the Korea National Health and Nutrition Examination Survey 2013–2018 database. From 47,217 subjects who participated in the survey between 2013 and 2018, only subjects over 40 years old were included. Subjects lacking 24‐h recall data and data on hypertriglyceridemia and body mass index, and who had implausible energy intake were excluded. A total of 19,806 participants' data were analyzed. Dietary data were based on 24‐h recall data, and dietary patterns were derived using factor analysis. Triglyceride levels greater than 200 mg/dl were considered hypertriglyceridemia, according to the Korean Society of Lipid and Atherosclerosis. Three dietary patterns— “oil and fats & seasoning”, “soybean paste and vegetable”, and “fruit and whole‐grain”— explained 7.9%, 6.3%, and 5.8% of variation in food intake, respectively. Comparing the lowest and highest dietary pattern score groups after adjusting for potential confounders revealed an inverse relationship between “fruit and whole‐grain” dietary pattern and hypertriglyceridemia in men (odds ratio [OR]: 0.61, 95% confidence interval [CI]: 0.45–0.82, p for trend <.0001); which was only marginal in women (OR: 0.78, 95% CI: 0.58–1.07, p for trend: .628). A diet containing high proportions of fruit and whole‐grain may have preventive effects on hypertriglyceridemia in middle and older aged Korean adults.

Consistently high TG levels may lead to changes in the composition and metabolism of low-and high-density lipoprotein (LDL and HDL) cholesterol, thereby causing an imbalance in serum cholesterol levels (Miller et al., 2011). Moreover, hypertriglyceridemia in conjunction with impaired fasting glucose is a well-known risk of the development of type 2 diabetes (D'Agostino et al., 2004). Since hypertriglyceridemia may affect other metabolic factors, it is currently considered a major risk factor for various chronic diseases.
For a long time, dietary control has been advocated for managing hypertriglyceridemia. Studies have examined the association between dietary factors and hypertriglyceridemia. According to a previous study, the TG level was expected to increase by 6% for every 5% decrease in the percent of total fat intake in those who consumed a low-fat and high-carbohydrate diet (Institute of Medicine, 2005).
Furthermore, studies have reported a link between the consumption of several food items and the development of hypertriglyceridemia (Guasch-Ferre et al., 2019;Takahashi et al., 2010;Yuan et al., 2015).
The consumption of more than three servings of fruits and vegetables and whole grains led to a reduction in TG levels in Brazilian adults (Takahashi et al., 2010). Additionally, a high intake of fruit, but not vegetables, was related to a decrease in the prevalence of elevated TG levels in Korean adults (Yuan et al., 2015). A meta-analysis of randomized controlled trials showed that the consumption of red meat resulted in a greater decrease in the level of TG than that of lowquality refined grains and simple sugars (Guasch-Ferre et al., 2019).
The dietary pattern analysis can be used as an adjunct method to explore the combined effect of nutrients and foods in a particular population and examine the relationship between overall diet and risk of metabolic diseases (Hu, 2002). In this regard, the association of dietary patterns with hypertriglyceridemia has been evaluated. A healthy dietary pattern, characterized by high consumption of whole grains, legumes, fruits, and vegetables, was inversely associated with low levels of TG in the Western population (Panagiotakos et al., 2007).
Moreover, a similar dietary pattern was negatively associated with fasting TG in a multiethnic Asian population (Whitton et al., 2018). Importantly, the relationship between specific dietary patterns and triglycerides has not been clearly elucidated in the Korean population. In a previous study involving Korean adults, a healthy dietary pattern, including grains, vegetables, and fish, was associated with a lower risk of hypertriglyceridemia than a traditional dietary pattern (Kim & Jo, 2011), while in another similar study, it showed a nonsignificant relationship (Song & Joung, 2012). Therefore, we aimed to derive dietary patterns and explore the relationship between dietary patterns and hypertriglyceridemia in the Korean adult population using data from a representative national survey in Korea.

| Study population
In this study, we utilized the database of the Korea National 2018-01-03-P-A). Among the 47,217 subjects who participated in the survey between 2013 and 2018, subjects who were less than 40 years old (n = 20,420) and lacked 24-h recall data (n = 3068), data on hypertriglyceridemia (n = 2657) and body mass index (BMI) (n = 49) were excluded. In addition, 1217 subjects who had implausibly high (male, >5000 kcal/day; female, >3500 kcal/day) or low F I G U R E 1 Flow diagram of analytical samples in this study: Korea National Health and Nutrition Examination Survey 2013-2018 (male, <500 kcal/day; female, <800 kcal/day) energy intake were excluded. Finally, a total of 19,806 participants' data were included in the analysis (Figure 1).

| Dietary intake and dietary pattern
Dietary intake and the dietary patterns were based on the 24-h recall data. Data on intake of major macronutrients, carbohydrate, protein, and fat were obtained and percentage energy from these macronutrient intakes was assessed as follows: macronutrient intake (g/day) * kcal/g (carbohydrate and protein: 4 kcal/g, fat: 9 kcal/g)/total energy intake (kcal/day). The food items were categorized into 24 food groups based on the similarity of food type and nutrient composition. The specific food components of each food group are described in Table S1. Using factor analysis, different dietary patterns were identified from daily food intake within each food group. Principal component analysis was conducted to identify the distinct dietary patterns. The number of factors was determined using eigenvalues >1.3 and scree plots. The factor score for each dietary pattern was calculated through the sum of food intake weighted by their factor loadings. Three factors with high positive loadings were used to derive and label dietary patterns: "oil and fats & seasoning," "soybean paste and vegetable," and "fruit and whole-grain." The subjects were divided into three groups based on their dietary pattern scores.

| Covariates
Sociodemographic and health-related behavior data, including household income level, physical activity, alcohol consumption, and smoking were obtained via a self-administered questionnaire.
Household income level was classified as low, medium-low, mediumhigh, and high. Physical activity status was defined according to the frequency of walking and categorized as none, <3 days/week, and 4-7 days/week. Current alcohol consumption was determined as the presence or absence of alcohol intake in the recent 1 year ("yes" and "no"). Based on the smoking status, the subjects were categorized as "non-smokers" and "smokers." Height and weight were measured using standard protocol by trained staff. BMI was calculated as the weight divided by the square of the height (kg/m 2 ).

| Statistical analysis
Statistical analyses were performed using SAS software (version 9.4; SAS Institute, Inc.). Statistical significance was set at p < .05.
Categorical data were presented as numbers and percentages and continuous data as means with standard error. week, and 4-7 days/week). Model 3 was additionally adjusted for energy-adjusted carbohydrate (continuous) using the residual method (Willett & Stampfer, 1986).

| RE SULTS
The factor loadings for three dietary patterns are shown in Table 1.
The "oil and fats & seasoning" pattern included high consumption of oil and fats, seasoning, egg, flour, and low consumption of white rice.
The "soybean paste and vegetable" pattern included high consumption of soybean paste, vegetables, fish and seafood, kimchi, and low consumption of pizza, hamburger, bread, sandwich, cereal, and dairy products. The "fruit and whole-grain" pattern included high consumption of fruit, whole grains, dairy products, potato, and low consumption of meat, alcoholic beverages, and white rice.
The general characteristics of this study population according to quantiles of three pattern scores are described in Table 2. The "oil and fats & seasoning" dietary pattern was positively associated with men who were younger, more active, and had higher alcohol intake, and women who were younger and smoked and consumed alcohol frequently. The "soybean-paste and vegetable" dietary pattern group included men who were old and tended to drink and smoke often and women who were old and smoked and consumed alcohol infrequently. Likewise, the "fruit and whole-grain" dietary pattern group included men in a high-income household who also smoked and consumed alcohol infrequently and women who were young, active, and smoked and consumed alcohol infrequently.
The energy and the macronutrient intake according to three dietary pattern scores are presented in Table 3. The participants following the "oil and fats & seasoning" dietary pattern tended to have high energy, carbohydrate, protein, and fat intake and high percentage of energy from protein and fat intake in both men and women.
The participants following the "soybean paste and vegetable" dietary

| DISCUSS ION
In this study, using data from 2013-2018 KNHANES, a negative relationship was observed between the "fruit and whole-grain" dietary pattern and hypertriglyceridemia in middle and older aged Korean adults. Among men following the "fruit and whole-grain" pattern, the highest dietary pattern score group was significantly associated with a 39% lower prevalence of hypertriglyceridemia than the lowest dietary pattern score group. Among women, there was a marginal negative association between hypertriglyceridemia and "fruit and whole-grain" dietary pattern.
The assessment of dietary patterns rather than a single nutrient or specific food intake is known to be a better approach to evaluate the association of overall diet with chronic diseases in a population. As described above, fruit consumption is generally included in healthy dietary patterns to control cardiometabolic parameters (Panagiotakos et al., 2007). Indeed, a high intake of fruits was negatively associated with hypertriglyceridemia in a recent meta-analysis (Kodama et al., 2018). In addition, increased frequency of fruit consumption (≥3-4 servings/day) was negatively associated with hypertriglyceridemia in the Asian and South American populations (Lim & Kim, 2020;Takahashi et al., 2010). The consumption of total fruit and specific fruit subgroups, such as citrus, noncitrus, and carotenerich fruits, also showed an inverse association with hypertriglyceridemia in an observational study (Yuan et al., 2015). In an intervention study, grapefruit supplementation led to a decrease in serum TG in hyperlipidemic patients (Gorinstein et al., 2006).
However, the association between fruit intake and hypertriglyceridemia should be interpreted with caution since a high amount of fructose in fruits may lead to an increase in blood TG levels (Sharma et al., 2016). Dietary fructose led to an increase in postprandial TG levels in the short term, controlled feeding studies (Schaefer et al., 2009), and intake of only vegetables, not fruit, was related to a reduced risk of type 2 diabetes mellitus, which has been linked to hypertriglyceridemia (Colditz et al., 1992;Villegas et al., 2008;Williams et al., 1999), indicating that fruits and vegetables rich in phytochemicals or fibers have an antihypertriglyceridemia effect

TA B L E 3 (Continued)
TA B L E 4 The odds ratios of hypertriglyceridemia across the quantiles of three dietary pattern scores among middle and older aged Koreans, the 2013-2018 KNHANES that is attenuated by fructose (Kodama et al., 2018). Therefore, we evaluated energy-adjusted carbohydrate intake to exclude the potential confounding effects of simple sugar intake. The results suggesting a favorable effect of fruit intake on hypertriglyceridemia in this study can be useful evidence for a dietary recommendation.
Whole-grain consumption also plays a potential role in the prevention of hypertriglyceridemia. In a 12-week nutritional intervention study, a whole grain cereal-based diet led to a greater decrease in postprandial TG levels than a refined cereal diet (Giacco et al., 2014).
In another randomized crossover study, a lower value for incremental area under the curve for TG level was observed in subjects on a whole-grain diet with dairy, chicken, and nuts than in subjects on a refined grain diet with red meat . Meanwhile, a whole-grain diet also had favorable effects on other lipid profiles.
According to Giacco et al., intake of whole-meal wheat foods for 3 weeks significantly reduced postprandial plasma LDL cholesterol in their randomized clinical study (Giacco et al., 2010). In a metaanalysis of randomized controlled studies, whole-grain diets led to a greater decrease in total and LDL cholesterol than nonwhole-grain diets (Hollaender et al., 2015).
In particular, the consumption of a whole-grain diet can be an Indeed, white rice consumption was positively associated with the prevalence of dyslipidemia in Korean adults (Song & Song, 2019).
In addition, among subjects following the "Korean healthy" dietary pattern, characterized by whole grains, legumes, vegetables, and fruits, the highest score group showed significantly lower TG levels than the lowest score group, while among the subjects following the "rice and vegetables" dietary pattern, consisting of white rice, vegetables, and eggs, showed no significant relationship with triglyceride levels in Korean population with type 2 diabetes (Lim et al., 2011).
In summary, the whole grain dietary pattern can play a major role in preventing hypertriglyceridemia among Koreans who consume a large amount of rice-based carbohydrate-rich food items.
However, the mechanism underlying the negative correlation between triglyceride level and whole-grain diet remains unclear.
Nevertheless, dietary fibers in whole grain appear to reduce blood lipid levels. In particular, the viscous fibers, such as β-glucans, a major nutrient of whole grains, including barley and oat, have shown hypocholesterolemic effects (Tosh & Bordenave, 2020). In addition, whole grain consumption may result in either lipoprotein lipase activation or synthesis of these lipoproteins and induce a decrease in postprandial TG levels (Frayn, 2002;Giacco et al., 2014). Further studies exploring the effect of whole grain and its components on TG levels are required.
To the best of our knowledge, this is the first study to reveal the inverse association between hypertriglyceridemia and the "fruit and whole-grain" dietary pattern in a nationally representative sample of the middle-aged and older aged Korean adult population.
However, several limitations exist in this study. First, the 1-day, 24-h dietary recall method, which was used for dietary assessment in KNHANES, may not accurately reflect the usual dietary intake and its long-term effect in subjects. Second, several decisions used in the factor analysis, such as the number of extracted dietary pattern groups, categorization of food items into food groups, and the rotation method, can be subjective (Martinez et al., 1998). Finally, this study was not able to examine the causal relationship between dietary pattern and hypertriglyceridemia due to the cross-sectional study design of KNHANES. In addition, despite adjusting for confounding variables, there may have been potential confounding bias due to the observational study design of this study. These reasons may limit the possibility of generalizing the results. Therefore, additional studies with different study designs, such as clinical or prospective cohort study are required to confirm the causal relationship of the "fruit and whole-grain" dietary pattern with hypertriglyceridemia.

| CON CLUS IONS
This study among middle and older aged Korean adults found that the "fruit and whole-grain" dietary pattern was associated with a significantly low prevalence of hypertriglyceridemia in men, whereas the effect was only marginal in women. Our findings indicate that a high proportion of fruit and whole grain in a diet may prevent hypertriglyceridemia in middle and older aged Korean adults.

CO N FLI C T O F I NTE R E S T
The authors declare that they do not have any conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data are available in a public, open access repository. Website: https://knhan es.kdca.go.kr/knhan es/eng/index.do.